{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,26]],"date-time":"2026-02-26T19:59:27Z","timestamp":1772135967946,"version":"3.50.1"},"reference-count":99,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,10,17]],"date-time":"2017-10-17T00:00:00Z","timestamp":1508198400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,10,17]],"date-time":"2017-10-17T00:00:00Z","timestamp":1508198400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    <jats:italic>Wolbachia pipientis<\/jats:italic>\n                    is an intracellular endosymbiont infecting many arthropods and filarial nematodes. Little is known about the short-term evolution of\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    or its interaction with its host.\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    is maternally inherited, resulting in co-inheritance of mitochondrial organelles such as mtDNA. Here I explore the evolution of\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    , and the relationship between\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    and mtDNA, using a large inbred panel of\n                    <jats:italic>Drosophila simulans<\/jats:italic>\n                    . I compare this to the only other large population genomic\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    dataset from\n                    <jats:italic>D<\/jats:italic>\n                    .\n                    <jats:italic>melanogaster<\/jats:italic>\n                    . I find reduced diversity relative to expectation in both\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    and mtDNA, but only mtDNA shows evidence of a recent selective sweep or population bottleneck. I estimate\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    and mtDNA titre in each genotype, and I find considerable variation in both phenotypes, despite low genetic diversity in\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    and mtDNA. A phylogeny of\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    and of mtDNA suggest a recent origin of the infection derived from a single origin. Using\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    and mtDNA titre as a phenotype, I perform the first association analysis using this phenotype with the nuclear genome and find several implicated regions, including one which contains four CAAX-box protein processing genes. CAAX-box protein processing can be an important part of host-pathogen interactions in other systems, suggesting interesting directions for future research.\n                  <\/jats:p>","DOI":"10.1038\/s41598-017-13901-3","type":"journal-article","created":{"date-parts":[[2017,10,11]],"date-time":"2017-10-11T08:00:03Z","timestamp":1507708803000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Population genomics of Wolbachia and mtDNA in Drosophila simulans from California"],"prefix":"10.1038","volume":"7","author":[{"given":"Sarah","family":"Signor","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2017,10,17]]},"reference":[{"key":"13901_CR1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0038544","volume":"7","author":"R Zug","year":"2012","unstructured":"Zug, R. & Hammerstein, P. Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS ONE \n                           7, e38544 (2012).","journal-title":"PLoS ONE"},{"key":"13901_CR2","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1111\/j.1574-6968.2008.01110.x","volume":"281","author":"K Hilgenboecker","year":"2008","unstructured":"Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A. & Werren, J. H. How many species are infected with Wolbachia?\u2013A statistical analysis of current dat. a. FEMS Microbiol. Lett. \n                           281, 215\u2013220 (2008).","journal-title":"a. FEMS Microbiol. Lett."},{"key":"13901_CR3","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1046\/j.1365-2583.2000.00203.x","volume":"9","author":"A Jeyaprakash","year":"2000","unstructured":"Jeyaprakash, A. & Hoy, M. A. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol. Biol. \n                           9, 393\u2013405 (2000).","journal-title":"Insect Mol. Biol."},{"key":"13901_CR4","doi-asserted-by":"crossref","first-page":"1319","DOI":"10.1093\/genetics\/140.4.1319","volume":"140","author":"M Turelli","year":"1995","unstructured":"Turelli, M. & Hoffmann, A. A. Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics \n                           140, 1319\u20131338 (1995).","journal-title":"Genetics"},{"key":"13901_CR5","doi-asserted-by":"crossref","first-page":"713","DOI":"10.1093\/genetics\/132.3.713","volume":"132","author":"M Turelli","year":"1992","unstructured":"Turelli, M., Hoffmann, A. A. & McKechnie, S. W. Dynamics of cytoplasmic incompatibility and mtDNA variation in natural Drosophila simulans populations. Genetics \n                           132, 713\u2013723 (1992).","journal-title":"Genetics"},{"key":"13901_CR6","doi-asserted-by":"publisher","first-page":"1735","DOI":"10.1111\/j.0014-3820.2002.tb00187.x","volume":"56","author":"S Charlat","year":"2002","unstructured":"Charlat, S., Nirgianaki, A., Bourtzis, K. & Mer\u00e7ot, H. Evolution of Wolbachia-induced cytoplasmic incompatibility in Drosophila simulans and D. sechellia. Evolution \n                           56, 1735\u20131742 (2002).","journal-title":"Evolution"},{"key":"13901_CR7","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1098\/rspb.1992.0023","volume":"247","author":"F Rousset","year":"1992","unstructured":"Rousset, F., Vautrin, D. & Solignac, M. Molecular identification of Wolbachia, the agent of cytoplasmic incompatibility in Drosophila simulans, and variability in relation with host mitochondrial types. Proc. R. Soc. B \n                           247, 163\u2013168 (1992).","journal-title":"Proc. R. Soc. B"},{"key":"13901_CR8","doi-asserted-by":"crossref","first-page":"933","DOI":"10.1093\/genetics\/126.4.933","volume":"126","author":"AA Hoffmann","year":"1990","unstructured":"Hoffmann, A. A., Turelli, M. & Harshman, L. G. Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics \n                           126, 933\u2013948 (1990).","journal-title":"Genetics"},{"key":"13901_CR9","doi-asserted-by":"publisher","first-page":"1413","DOI":"10.1098\/rspb.2002.2022","volume":"269","author":"C Berticat","year":"2002","unstructured":"Berticat, C., Rousset, F., Raymond, M., Berthomieu, A. & Weill, M. High Wolbachia density in insecticide-resistant mosquitoes. Proc. R. Soc. B \n                           269, 1413\u20131416 (2002).","journal-title":"Proc. R. Soc. B"},{"key":"13901_CR10","doi-asserted-by":"publisher","first-page":"e25430","DOI":"10.1371\/journal.pone.0025430","volume":"6","author":"ZS Wong","year":"2011","unstructured":"Wong, Z. S., Hedges, L. M., Brownlie, J. C. & Johnson, K. N. Wolbachia-mediated antibacterial protection and immune gene regulation in Drosophila. PLoS ONE \n                           6, e25430\u20139 (2011).","journal-title":"PLoS ONE"},{"key":"13901_CR11","doi-asserted-by":"publisher","first-page":"e1000656","DOI":"10.1371\/journal.ppat.1000656","volume":"5","author":"SE Osborne","year":"2009","unstructured":"Osborne, S. E., Leong, Y. S., O\u2019Neill, S. L. & Johnson, K. N. Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog \n                           5, e1000656\u20139 (2009).","journal-title":"PLoS Pathog"},{"key":"13901_CR12","doi-asserted-by":"publisher","first-page":"791","DOI":"10.1098\/rspb.2005.3383","volume":"273","author":"A Fytrou","year":"2006","unstructured":"Fytrou, A., Schofield, P. G., Kraaijeveld, A. R. & Hubbard, S. F. Wolbachia infection suppresses both host defence and parasitoid counter-defence. Proc. R. Soc. 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PLoS Biol. \n                           6, e1000002 (2008).","journal-title":"PLoS Biol."},{"key":"13901_CR15","doi-asserted-by":"publisher","DOI":"10.1126\/science.1162418","volume":"322","author":"LM Hedges","year":"2008","unstructured":"Hedges, L. M., Brownlie, J. C. & O\u2019Neill, S. L. Wolbachia and virus protection in insects. Science \n                           322, 702 (2008).","journal-title":"Science"},{"key":"13901_CR16","doi-asserted-by":"crossref","unstructured":"Jiggins, F. M., Hurst, G. & Majerus, M. Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host B. Proc. R. Soc. B \n                           267, 69\u201373 (2000).","DOI":"10.1098\/rspb.2000.0968"},{"key":"13901_CR17","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1111\/j.0014-3820.2006.tb01084.x","volume":"60","author":"K Koukou","year":"2006","unstructured":"Koukou, K. et al. Influence of antibiotic treatment and Wolbachia curing on sexual isolation among Drosophila melanogaster cage populations. Evolution \n                           60, 87\u201311 (2006).","journal-title":"Evolution"},{"key":"13901_CR18","doi-asserted-by":"publisher","first-page":"440","DOI":"10.1038\/353440a0","volume":"353","author":"M Turelli","year":"1991","unstructured":"Turelli, M. & Hoffmann, A. A. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature \n                           353, 440\u2013442 (1991).","journal-title":"Nature"},{"key":"13901_CR19","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1093\/genetics\/119.2.435","volume":"119","author":"AA Hoffmann","year":"1988","unstructured":"Hoffmann, A. A. & Turelli, M. Unidirectional incompatibility in Drosophila simulans: inheritance, geographic variation and fitness effects. Genetics \n                           119, 435\u2013444 (1988).","journal-title":"Genetics"},{"key":"13901_CR20","doi-asserted-by":"publisher","first-page":"692","DOI":"10.1111\/j.1558-5646.1986.tb00531.x","volume":"40","author":"AA Hoffmann","year":"1986","unstructured":"Hoffmann, A. A., Turelli, M. & Simmons, G. M. Unidirectional incompatibility between populations of Drosophila simulans. Evolution \n                           40, 692\u2013701 (1986).","journal-title":"Evolution"},{"key":"13901_CR21","doi-asserted-by":"publisher","first-page":"5725","DOI":"10.1073\/pnas.0810753106","volume":"106","author":"L Klasson","year":"2009","unstructured":"Klasson, L. et al. The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc. Nat. Acad. Sci. USA \n                           106, 5725\u20135730 (2009).","journal-title":"Proc. Nat. Acad. Sci. 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J Mol Evol \n                           51, 64\u201375 (2000).","journal-title":"J Mol Evol"},{"key":"13901_CR24","doi-asserted-by":"crossref","first-page":"1519","DOI":"10.1093\/genetics\/144.4.1519","volume":"144","author":"JW Ballard","year":"1996","unstructured":"Ballard, J. W., Hatzidakis, J., Karr, T. L. & Kreitman, M. Reduced variation in Drosophila simulans mitochondrial DNA. Genetics \n                           144, 1519\u20131528 (1996).","journal-title":"Genetics"},{"key":"13901_CR25","first-page":"461","volume":"317","author":"M Solignac","year":"1994","unstructured":"Solignac, M., Vautrin, D. & Rousset, F. Widespread occurence of the proteobacteria Wolbachia and partial cytoplasmic incompatibility in Drosophila melanogaster. C. R. Acad. Sci. \n                           317, 461\u2013479 (1994).","journal-title":"C. R. Acad. Sci."},{"key":"13901_CR26","first-page":"531","volume":"40","author":"M Solignac","year":"1986","unstructured":"Solignac, M. & Monnerot, M. Race formation, speciation, and introgression within Drosophila simulans, D. mauritiana, and D. sechellia inferred from mitochondrial DNA analysis. Evolution \n                           40, 531\u2013539 (1986).","journal-title":"Evolution"},{"key":"13901_CR27","doi-asserted-by":"publisher","first-page":"419","DOI":"10.1038\/hdy.1988.133","volume":"61","author":"F Baba-A\u00efssa","year":"1988","unstructured":"Baba-A\u00efssa, F., Solignac, M., Dennebouy, N. & David, J. R. Mitochondrial DNA variability in Drosophila simulans: quasi absence of polymorphism within each of the three cytoplasmic races. Heredity \n                           61, 419\u2013426 (1988).","journal-title":"Heredity"},{"key":"13901_CR28","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1093\/genetics\/129.2.399","volume":"129","author":"C Montchamp-Moreau","year":"1991","unstructured":"Montchamp-Moreau, C., Ferveur, J. F. & Jacques, M. Geographic distribution and inheritance of three cytoplasmic incompatibility types in Drosophila simulans. Genetics \n                           129, 399\u2013407 (1991).","journal-title":"Genetics"},{"key":"13901_CR29","doi-asserted-by":"publisher","first-page":"1661","DOI":"10.1111\/j.0014-3820.2000.tb00710.x","volume":"54","author":"AC James","year":"2000","unstructured":"James, A. C. & Ballard, J. W. Expression of cytoplasmic incompatibility in Drosophila simulans and its impact on infection frequencies and distribution of Wolbachia pipientis. Evolution \n                           54, 1661\u20131672 (2000).","journal-title":"Evolution"},{"key":"13901_CR30","doi-asserted-by":"publisher","first-page":"5765","DOI":"10.1111\/mec.12530","volume":"22","author":"AM Early","year":"2013","unstructured":"Early, A. M. & Clark, A. G. Monophyly of Wolbachia pipientis genomes within Drosophila melanogaster: geographic structuring, titre variation and host effects across five populations. Mol. Ecol. \n                           22, 5765\u20135778 (2013).","journal-title":"Mol. Ecol."},{"key":"13901_CR31","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1003129","volume":"8","author":"MF Richardson","year":"2012","unstructured":"Richardson, M. F. et al. Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster. PLoS Genet. \n                           8, e1003129 (2012).","journal-title":"PLoS Genet."},{"key":"13901_CR32","doi-asserted-by":"publisher","first-page":"2493","DOI":"10.1093\/molbev\/msn199","volume":"25","author":"MDS Nunes","year":"2008","unstructured":"Nunes, M. D. S. & Nolte, V. & Schl tterer, C. Nonrandom Wolbachia infection status of Drosophila melanogaster strains with different mtDNA haplotypes. Mol. Biol. Evol. \n                           25, 2493\u20132498 (2008).","journal-title":"Mol. Biol. 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H. & Aquadro, C. F. Recurrent positive selection at bgcn, a key determinant of germ line differentiation, does not appear to be driven by simple coevolution with its partner protein bam. Mol. Biol. Evol. \n                           24, 182\u2013191 (2006).","journal-title":"Mol. Biol. Evol."},{"key":"13901_CR36","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1005453","volume":"11","author":"HA Flores","year":"2015","unstructured":"Flores, H. A., Bubnell, J. E., Aquadro, C. F. & Barbash, D. A. The Drosophila bag of marbles gene interacts genetically with Wolbachia and shows female-specific effects of divergence. PLoS Genet. \n                           11, e1005453 (2015).","journal-title":"PLoS Genet."},{"key":"13901_CR37","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.0030190","volume":"3","author":"LR Serbus","year":"2007","unstructured":"Serbus, L. R. & Sullivan, W. A Cellular basis for Wolbachia recruitment to the host germline. PLoS Pathog \n                           3, e190 (2007).","journal-title":"PLoS Pathog"},{"key":"13901_CR38","doi-asserted-by":"publisher","first-page":"683","DOI":"10.1146\/annurev.genet.41.110306.130354","volume":"42","author":"LR Serbus","year":"2008","unstructured":"Serbus, L. R., Casper-Lindley, C., Landmann, F. & Sullivan, W. The genetics and cell biology of Wolbachia-host interactions. Annu. Rev. Genet. \n                           42, 683\u2013707 (2008).","journal-title":"Annu. Rev. Genet."},{"key":"13901_CR39","doi-asserted-by":"publisher","first-page":"2918","DOI":"10.1073\/pnas.052466499","volume":"99","author":"EA McGraw","year":"2002","unstructured":"McGraw, E. A., Merritt, D. J., Droller, J. N. & O\u2019Neill, S. L. Wolbachia density and virulence attenuation after transfer into a novel host. Proc. Nat. Acad. Sci. USA \n                           99, 2918\u20132923 (2002).","journal-title":"Proc. Nat. Acad. Sci. 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PLoS Biol. \n                           13, e1002065 (2015).","journal-title":"PLoS Biol."},{"key":"13901_CR45","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1003896","volume":"9","author":"E Chrostek","year":"2013","unstructured":"Chrostek, E. et al. Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: A phenotypic and phylogenomic analysis. PLoS Genet. \n                           9, e1003896 (2013).","journal-title":"PLoS Genet."},{"key":"13901_CR46","doi-asserted-by":"publisher","first-page":"454","DOI":"10.1038\/nature10356","volume":"476","author":"AA Hoffmann","year":"2011","unstructured":"Hoffmann, A. A. et al. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature \n                           476, 454\u2013457 (2011).","journal-title":"Nature"},{"key":"13901_CR47","doi-asserted-by":"publisher","first-page":"6963","DOI":"10.1128\/AEM.01038-08","volume":"74","author":"CJ McMeniman","year":"2008","unstructured":"McMeniman, C. J. et al. Host adaptation of a Wolbachia strain after long-term serial passage in mosquito cell lines. App. Environ. Microbiol. \n                           74, 6963\u20136969 (2008).","journal-title":"App. Environ. Microbiol."},{"key":"13901_CR48","doi-asserted-by":"publisher","first-page":"6922","DOI":"10.1128\/AEM.01727-12","volume":"78","author":"SE Osborne","year":"2012","unstructured":"Osborne, S. E., Iturbe-Ormaetxe, I., Brownlie, J. C., O\u2019Neill, S. L. & Johnson, K. N. Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. App. Environ. Microbiol. \n                           78, 6922\u20136929 (2012).","journal-title":"App. Environ. 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